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Dirge of Cerberus is a third-person shooter RPG. The game consists of 10 chapters with stages in each of them. Players will primarily play Vincent, though on one occasion, players will also play as Cait Sith.

As Vincent, players will shoot enemies by raising their weapon with L1 or R1, and then subsequently shoot again with R1 after setting an enemy in their sights with the right analog stick. A combo of melee attacks can also be performed to conserve ammunition and even deflect incoming bullets and rockets. Vincent can also loose an elementally-aligned magic bullet with L1 by equipping a Materia to the weapon. Vincent can also perform jumps and rush maneuver to quickly avoid attacks, although in the Japanese version, the rush was originally a simple roll. As Cait Sith, players must hide behind objects to prevent detection from Deepground soldiers while progressing through the level.

Gameplay in Dirge of Cerberus.

Defeating opponents earns players Experience, which can be used to level up Vincent for increased attributes or exchanged for gil at a x10 exchange rate after completing a chapter or restarting upon defeat. Vincent's weapons can also be customized with items bought or found throughout the game. Players can also use the Limit Breaker item to transform Vincent into his iconic Galian Beast, benefiting from increased attack and defense power and being able to shoot homing fireballs. In the Japanese version, the player was able to freely transform back and forth from the Galian Beast by pressing L1+R1, gradually consuming MP as you remained in Limit Break form. Vincent can also purchase items like Potions and Ethers from shops in between chapters or on the field from jukeboxes.

Dirge of Cerberus also supported the use of a USB mouse and keyboard for PC-like control, and a user-friendly sight support system, ranging from the normal "Manual" sight control for seasoned shooters, a "Semi-automatic" sight control allowing players to align an over-sized sight at enemies to lock a smaller sight onto them, and an "Automatic" sight control which locks onto the nearest enemy as soon as the gun is raised, perfect for players lacking the dexterity to accurately aim.

The Japanese version also featured an online multiplayer mode where a player could create a custom Deepground soldier and go head-to-head with other players, or work alongside them to complete missions that takes them all over the world of Final Fantasy VII. The multiplayer even included its own story, divulging more secrets about Deepground and the Tsviets prior to the Vincent's battle with them. While releases outside of Japan did not see the multiplayer, they did come packed with the Extra Mode, which featured a complete list of different Missions to tackle, many of which were missions from the multiplayer.

Three years after the events of Final Fantasy VII, an unknown group of powerful SOLDIERs appear, bringing a swift and bitter end to the peace enjoyed by the people of the world. The members of this enigmatic group are the Deepground SOLDIERs; an elite battalion of SOLDIER's finest who were trapped under the ruins of Midgar for three long years. Their intention is to call forth the final WEAPON, Omega, before its time. However, to do that, Deepground needs a mass of "clean" sacrifices, and the enigmatic Vincent to lead the way to Omega.

After Deepground begins their invasion of the sleepy town of Kalm, Vincent Valentine finds himself pursued by their elite members, the Tsviets. An unrelenting chain of events leads Vincent back to places he only wished he could forget, unraveling the truth behind his agonizing past, and forcing him to once again to be the key player in a battle for the planet itself, and all those living in it.

Reeve Tuesti, former Head of Urban Development at Shinra (as well as the remote pilot of Cait Sith), is now the leader of the World Regenesis Organization, or WRO, which is responsible for the reconstruction of the planet, as well as protecting it from those who wish the world further harm. Yuffie Kisaragi is another member of the organization, and several other characters from the original game provide the WRO with outside assistance.

Vincent meets Shalua Rui, a doctor with the WRO, whilst investigating the disappearance of WRO troops in the city of Edge, and during a confrontation with Rosso the Crimson, one of the Tsviets, he momentarily transforms into Chaos, attacking Rosso and forcing her to flee.

Vincent collapses and is taken to the WRO headquarters where he again meets Shalua. After learning that Lucrecia was involved in the Chaos project, the headquarters came under attack by Deepground troops, led by two of the Tsviets, Azul the Cerulean and Shelke the Transparent. Vincent successfully stopped the duo and Reeve holds them captive in the meantime. After the incidents at the WRO headquarters, Vincent leaves to Shinra building in Nibelheim, to search for Deepground, Reeve advises him to go through the sewers, as the path above is crawling with Deepground soldiers.

Reaching the Mansion through the sewers, Vincent is surprised to find a Hologram of Lucrecia waiting for him, apologizing again. She speaks of her scattered data on Omega which she has left in the mansion. After Vincent found the remaining data, he runs into Rosso again. Preparing to battle her, Rosso instead flees and sends a spider-like mecha, The Black Widow, after him, which Vincent destroys in the Mansion Foyer. Preparing to leave, Rosso ambushes Vincent and plunges her hand into his chest, retrieving the Protomateria, which is revealed to be what allows Vincent to control Chaos. Without it, it is possible for Chaos to overwhelm him. Rosso makes to kill Vincent, but a figure appears and tosses their shuriken at her. A flash bomb erupts, blinding Rosso momentarily and as the light dissipates, the mysterious figure rescues Vincent out of the mansion as Rosso yells "Wutai flea!". The mysterious figure is later revealed to be Yuffie. As Vincent is passed out, a flashback scene appears where he is discussing with Hojo about Lucrecia taking part in a project consisted of using Lucrecia's unborn child as an experiment for a Jenova project. Vincent narrates the following after the brief flashback is over; "That was my sin. And this... This... Is my punishment.".

He awakens later to find himself in a van with the mysterious figure,now known as Yuffie, sitting in front of him. She explains how she had found him "corpse-like" in the Shinra Manor and saves him from Rosso. Yuffie eventually brags on about her saving the great Vincent Valentine and asks for a thanks. Vincent, in return, take her words rather seriously and thanks her. She gets flustered, shaking her head, saying she did not mean for it to be taken seriously. Reeve soon contacts the two and says he has received Vincent's data which he collected earlier in Shinra Manor and requests for them to hurry to headquarters. At headquarters, Shelke awakes inside a tube of water to see Shalua slouched over her computer terminal asleep. Shalua rises to see Shelke conscious and the two discuss how Shalua will not allow Shelke to kill her in order to return to Deepground. Azul soon awakens once more and Deepground strikes back after their first failed attempt.

Vincent makes his way to WRO headquarters to see the building in chaos. Azul approaches Vincent in his beast form and almost kills Shelke had she not used a materia to paralyze and block his oncoming attack. Azul is keen on killing Shelke since Weiss has ordered her termination, as she was no longer useful to the Tsviets since they had now found what they have been looking for which was the Protomateria. Shalua, sensing the danger of the situation, opens a door for the three of them to escape. Shelke, reluctant to go through the door, has Shalua toss her through the small opening left by placing her robotic arm between the closing doors. She apologizes to Shelke that she was unable to be a better sister to her as Azul is slowly approaching them. Azul is seen in the background as the pressure from the doors destroy Shalua's arm. Vincent desperately tries to open the door, but it continues closing. Shalua exchanges some final words to Shelke and once the doors fully close, a loud thud is heard and beige-colored liquid seeps under the now closed doors.

Shalua is in a regeneration tube while Yuffie is explaining to Vincent and Shelke that she has suffered far too much trauma to her head and would most likely never awake again. Shelke calls Shalua a fool and is slapped by an enraged Yuffie. She leaves the room on the verge of tears. Vincent and Shelke share a meaningful conversation on how people risk their lives for the ones they deeply care about. Reeve comes into the room and explains that the Omega Report Vincent gave him were incomplete. Shelke then offers to use her Synaptic Net Dive ability to aid Reeve in making any sense of the report.

The remaining Tsviets excluding Weiss, along with Deepground soldiers, stand on the outskirts of Midgar ready for the attack from WRO troops. The members from Avalanche join in on the battle, assisting WRO. Meanwhile, Shelke is assisting in her own way by helping command WRO members when to drop, informing Cid of conditions of the airships, and so on. Vincent is riding on a hoverboard-like device and successfully lands in Midgar, looking up at Shinra Tower. He makes it to the top of Shinra Tower only to meet Rosso the Crimson. The two engage in battle where Vincent comes out as victor. Rosso, not wanting Vincent to have the pleasure in defeating her, slices off the platform she stood on and falls to her death as she is cackling maniacally.

Vincent's phone rings and he picks it up to find Shelke on the other line. She gives him directions to infiltrate Deepground. As he is talking, he feels a pain in his chest and collapses, nearly transforming into Chaos. He asks why Chaos is acting up and receives an answer from Shelke explaining to him that the Protomateria was what kept him in control of Chaos. The two hang up and soon afterward, Nero appears in the Shera's engine room and destroys one or two of the engines. Cid questions what is happening as Shelke runs into the room and confronts Nero. He leaves in a dark portal.

As Vincent continues to delve deeper to the heart of Deepground, he receives a call from Tifa. He answers and hears the voices of most of his friends. Tifa sends Vincent a map of the Shinra building. They hang up and Vincent continues onward. He eventually reaches an elevator with Azul standing on it. They engage in yet another fight where Azul is in his beast form once more. Vincent comes out triumphant but as Chaos. Chaos sends Azul off the elevator and laughs maniacally as Azul tumbles to his death. There is another flashback where Vincent is inside a regenerative tube with Lucrecia in the lab. Hojo comes into the lab and begins laughing, suggesting she is using Vincent as an experiment for Omega and Chaos while she frantically denies it.

Another flashback appears where it is showing Lucrecia and Grimoire Valentine, Vincent's father, in a laboratory and a ball of black energy inside a regenerative tube expands, filling the tube and cracks it. Grimoire shoves Lucrecia out of the way as the dark energy hits him. The scene changes where he is lying on the ground with Lucrecia by his side as he dies. He tells her it was his time to return to the Lifestream and asks her to apologize to his son for him. Shelke is apparently seeing all of this and comments that he is simply returning to the planet. She soon remembers the time her mother had passed away and is comforted by Shalua, being told that her mother has only returned to the planet. Whether dreaming or hallucinating, she sees Shalua and is asked by her if it was okay for her to return to the planet. Shelke responds by telling her not yet and that the two still needed to catch up. She wakes up with tears rolling down her cheeks.

Vincent continues through Deepground's complex and meets with Nero. He asks Nero what he has done with Shelke and responds by saying she is inside him, trapped in darkness. He engulfs Vincent in the darkness as well but Vincent is unaffected. Shelke is within a cracked shield-bubble, losing hope. When she looks up, she sees Vincent and he rescues her. Nero watches and begins forming a cloud of darkness. Yuffie appears in her "mysterious ninja" garb on a tall building once more and begins giving a rather long speech about herself as a hero. It ends with her falling off the building, ruining the rather tense moment. Nero leaves saying his brother calls him.

Shelke is put inside a regenerative tube and Yuffie runs off to shut down the reactor. Vincent has yet another flashback about when he finds about how Lucrecia knew about his father. She starts crying saying that she didn't mean for him to die. Vincent is then left in the shadows while she runs off and confesses her love for Hojo. After his flashback, Shelke and Vincent have a strong conversation about the battle that they are fighting.

Vincent meets up with Yuffie, who had successfully shut down the reactor. They continue onward where they finally meet Weiss, the Deepground leader. But he appears to be unconscious. Yuffie thought that he was dead. They see Nero again who explains that Weiss would not be dead for long, and would be received a new life soon. Suddenly, the ground seems to shake and Vincent and Yuffie pull out their weapons. Nero, protective of his sibling, consumes them in darkness. Yuffie, who falls in darkness, begins to have a large headache and is almost consumed by darkness completely but is swiftly saved by Vincent who carries her out of the dark.

Nero returns again and explains his powers with the darkness. Vincent is then transported a different dimension-world in which he is to battle a spider mecha, controlled by Nero. After defeating the spider, Vincent faces Nero. Vincent comes out victorious but Nero staggers away in the real world through an open doorway.

Vincent proceeds to finally see an awakened Weiss. Nero happily goes to his brother but Weiss plunges his hand into his stomach, saying that he doesn’t need him anymore. Weiss then reveals himself to Vincent saying that it has been a long time since he saw him. Vincent is confused and Weiss reveals that he was reborn through data in his mind. Vincent then realizes that Weiss was he long-time enemy, Hojo.

Weiss/Hojo then has a speech about how he used Vincent as an experiment to hold in Chaos, how he founded Deepground, and how his experiment with Vincent could possibly work the same with Omega. Vincent fires his gun saying that he heard enough and battles Weiss. Weiss however is victorious on this fight. Vincent battles Weiss yet again, only to fail. Vincent almost transforms into Chaos but holographic Lucrecia stops him from doing so, saying that he needs to control it. He succeeds in doing so and maintains Chaos’s power while in his human form.

Vincent manages to stop the Hojo inside Weiss using Chaos. A dark Nero then appears in front of Weiss who says that they should merge together so that they may never be torn apart. Hojo tries to stop Weiss from leaving saying that it is his body but Weiss leaves with Nero to stop Hojo from making any other plots, ever. Yuffie runs in saying that they finally won, but before leaving, the reactor turns on from inside. Vincent pushes Yuffie away to be hit by the power. The entire Shinra building then transforms into a colossal machine, Omega. Vincent is turned into Chaos during the process.

Shelke, who had awoken and had escaped from the tube, performs SND, retrieves the Protomateria (from a figure that appears to be Lucrecia), and gives it back to Vincent. Vincent has yet another flashback of when Lucrecia tries to save him from decaying. She has flashbacks of her own about how Hojo found Vincent and thought she was experimenting with him and when she found Vincent collapsed on the floor after being shot by Hojo. She stopped the decaying of the tissue but instead he transformed into Chaos. She found Protomateria on the floor during his transformation and tried without success to try and find a way to stop the Chaos inside Vincent. After giving birth to her child, she tries to force Hojo to let her see her baby. She is then last seen apologizing to Vincent.

Vincent retrieves Shelke and places her on solid ground. Then he summons a large gun and flies off to stop Omega. Cloud, Tifa and Barrett manage to shut down the reactors that give Omega power and look to Vincent to do the rest of the work. Vincent dives inside of Omega and manages to destroy its power sources from the inside. Vincent then again dives into Omega from outside and faces Weiss again. Vincent wins again.

However, in order to stop Omega from leaving the planet with the Lifestream, Vincent forces himself to dive into Omega and force it back. However, in the process, Vincent had disintegrated. Vincent's location at this point is unknown. Back at 7th Heaven, Shelke now lives with Tifa and is seen sending a text to Vincent. The scene fades from Shelke sitting outside with Red XIII to Vincent, alive, sitting in the Crystal Cave. He says to Lucrecia that Chaos and Omega had returned to the planet and thanks her. While he exits the cave, Lucrecia is seen in the crystal with a tear rolling down her cheek. Vincent goes outside and meets with Shelke out in the field. Shelke said that everyone was waiting for him. They are last seen smiling together. The player then sees a figure near the moon that appears to be Omega, frozen in the sky.

The Multiplayer Mode storyline takes place at an unknown time before the start of the game. During this time in Deepground, the organization is not lead by the Tsviets but rather the cruel Restrictor who constantly tortures his test subjects to create the perfect killing machines. None of the other Deepground soldiers can fight against him, for they have a chip in their brain which restricts their actions. The storyline follows the training of a playable Tsviet (gender chosen by the player). During the soldier's training he or she meets up and fights with the other Tsviets while being led along by a mysterious SOLDIER named Usher. Though the player character's memory has been erased, he or she remembers a younger sister who was kidnapped along with them into Deepground. As the player advances, they eventually reach the rank of Tsviet, but are never actually given a color.

During a training exercise, the player joins with the Tsviets in a revolt against the Restrictor. Despite all their combined power, the Restrictor is still a formidable foe, and he is able to defeat several of them at once. But the player character has yet to have a chip implanted, so with his or her help the Tsviets prove victorious and they kill the Restrictor. In the end, however, the player learns that he or she has been misled. All memories they had of their sister had been implanted by Shelke using the SND. Even Usher was just a computer simulation who did not actually exist. The hope was that the player would take the Restictor's place so that Shinra would not notice the revolt, but the player character's mind had already collapsed. The Multiplayer Mode ends with his or her death.

Dirge of Cerberus' soundtrack was released in Japan on January 15, 2005. The soundtrack was composed by Masashi Hamauzu. Two theme songs on the soundtrack, "LONGING" and "REDEMPTION", were done by Japanese rock singer Gackt Camui. Gackt makes a "cameo" as Genesis in the game's secret ending.

An idea to make a Final Fantasy First-person shooter game was originally conceived by Producer Yoshinori Kitase. Before the game was to decided to be placed in the Final Fantasy VII universe, several other candidates were considered for the main protagonist like Irvine Kinneas from Final Fantasy VIII and Yuna from Final Fantasy X. Barret Wallace was also considered but Kitase eventually chose Vincent because the character "made a presence" in his mind.

The POV of the game was decided to be placed behind Vincent for a full-character view so that new-comers to the shooter genre would have an easier time adjusting to the gameplay. For this same reason an "Easy" mode was included.

Due to a rather negative reception in Japan and the developer's own dissatisfaction with the original version, the game's system was given an overhaul in between international release. The state goal of these changes was to make the game more single-player oriented. Changes include:

The aiming perspective has been shifted from an over-the-shoulder view to one behind Vincent for easier navigation of the surroundings.

Weapons can be customized to be lighter, so draw-times are quicker.

Vincent runs 1.2X faster.

He can perform a double-jump while mid-air. However, the environments are unchanged, so despite a higher jump, the player often cannot reach areas within range.

Attacks can be performed in the air.

Vincent's dodge roll was replaced by a dash move.

Limit Breaks do not take away from the Magic Bar; instead, they are started by an item called the "Limit Breaker".

"Easy Mode" is gone, replaced by an "Extra Hard Mode". In the Extra Hard Mode, players can unlock numerous things such as 40 extra missions, character models, a music player, and an artwork gallery.

The Multiplayer Mode has been removed. Several missions from it have been placed into the game as extra missions, but all storyline elements are absent.

In addition Dirge of Cerberus -Final Fantasy VII- International was released by Square Enix in Japan on September 4, 2008. The version retains all of the new features incorporated into the North American and European releases, and also includes the cutscenes that were originally only available in the Japanese online Multiplayer Mode. Audio is in English, with Japanese text and subtitles.